Evolution of the Rdr1 TNL-cluster in roses and other Rosaceous species

Abstract

BackgroundThe resistance of plants to pathogens relies on two lines of defense: a basal defense response and a pathogen-specific system, in which resistance (R) genes induce defense reactions after detection of pathogen-associated molecular patterns (PAMPS). In the specific system, a so-called arms race has developed in which the emergence of new races of a pathogen leads to the diversification of plant resistance genes to counteract the pathogens’ effect. The mechanism of resistance gene diversification has been elucidated well for short-lived annual species, but data are mostly lacking for long-lived perennial and clonally propagated plants, such as roses. We analyzed the rose black spot resistance gene, Rdr1, in five members of the Rosaceae: Rosa multiflora, Rosa rugosa, Fragaria vesca (strawberry), Malus x domestica (apple) and Prunus persica (peach), and we present the deduced possible mechanism of R-gene diversification.ResultsWe sequenced a 340.4-kb region from R. rugosa orthologous to the Rdr1 locus in R. multiflora. Apart from some deletions and rearrangements, the two loci display a high degree of synteny. Additionally, less pronounced synteny is found with an orthologous locus in strawberry but is absent in peach and apple, where genes from the Rdr1 locus are distributed on two different chromosomes. An analysis of 20 TIR-NBS-LRR (TNL) genes obtained from R. rugosa and R. multiflora revealed illegitimate recombination, gene conversion, unequal crossing over, indels, point mutations and transposable elements as mechanisms of diversification.A phylogenetic analysis of 53 complete TNL genes from the five Rosaceae species revealed that with the exception of some genes from apple and peach, most of the genes occur in species-specific clusters, indicating that recent TNL gene diversification began prior to the split of Rosa from Fragaria in the Rosoideae and peach from apple in the Spiraeoideae and continued after the split in individual species. Sequence similarity of up to 99% is obtained between two R. multiflora TNL paralogs, indicating a very recent duplication.ConclusionsThe mechanisms by which TNL genes from perennial Rosaceae diversify are mainly similar to those from annual plant species. However, most TNL genes appear to be of recent origin, likely due to recent duplications, supporting the hypothesis that TNL genes in woody perennials are generally younger than those from annuals. This recent origin might facilitate the development of new resistance specificities, compensating for longer generation times in woody perennials.

Genetic diversity and pathogenicity of Sphaceloma rosarum (teleomorph Elsinoë rosarum) causing spot anthracnose on roses

“…Determining whether resistance against spot anthracnose is controlled by a single locus or multiple loci has yet to be investigated and is outside of the scope of the present study. In addition, the transgenic rose genotype PC-RGA1, which expresses muRdr1A, one of the nine TNL-NBS-LRR genes in the Rdr1 locus (Terefe-Ayana et al, 2012), was susceptible to all of the isolates used in this study. Recent experiments suggest that muRdr1A is the active gene in race-specific interactions against black spot isolate DortE4 and several other isolates (T. Debener, unpublished data).…”

Genome-Wide Association Analysis of the Anthocyanin and Carotenoid Contents of Rose Petals

“…Therefore, we used two related rosaceous genomes assuming sufficient microsynteny to the rose genome: the very closely related genome of strawberry and the peach genome, which represents the next-closest relative (Shulaev et al, 2008). In several conventional marker mapping studies, strawberry was shown to be highly similar in its genome structure and marker order with only minor differences to roses (Gar et al, 2011; Spiller et al, 2011; Terefe-Ayana et al, 2012). This strategy proved informative, as we found a couple of clear clusters of significantly associated SNPs in both genomes.…”

Analysis of the Rdr1 gene family in different Rosaceae genomes reveals an origin of an R-gene cluster after the split of Rubeae within the Rosoideae subfamily

“…The rose genome displays extensive synteny with the Fragaria vesca genome with only two major rearrangements [9]. Synteny between Fragaria and Rosa genes has been observed for TNL genes (TIR (Drosophila Toll and mammalian interleukin (IL)-1 receptors), NBS (nucleotide-binding site) and LRR (leucine-rich repeat)) [10].…”